Global pollinator declines: trends, impacts and drivers

● Ashman, T.L. et al. (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85, 2408–2421 ● Aguilar, R. et al. (2006) Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecol. Lett. 9, 968–980 ● Klein, A.M. et al. (2007) Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. London B. Biol. Sci. 274, 303–313 ● Ricketts, T.H. et al. (2008) Landscape effects on crop pollination services: are there general patterns? Ecol. Lett. 11, 499–515 ● Ghazoul, J. (2005) Buzziness as usual? Questioning the global pollination crisis. Trends Ecol. Evol. 20, 367–373 ● Natural Research Council (2006) Status of Pollinators in North America, National Academic Press ● vanEngelsdorp, D. et al. (2008) A survey of honey bee colony losses in the U.S., Fall 2007 to Spring 2008. PLoS ONE 3, e4071. DOI:10.1371/ journal.pone.0004071 ● Potts, S.G. et al. (2010) Declines of managed honeybees and beekeepers in Europe? J. Apic. Res. 49, 15–22 ● Sammataro, D. et al. (2000) Parasitic mites of honey bees: life history, implications, and impact. Annu. Rev. Entomol. 45, 519–548 ● Kraus, B. and Page, R.E. (1995) Effect of Varroa jacobsoni (Mesostigmata: Varroidae) on feral Apis mellifera (Hymenoptera: Apidae) in California. Environ. Entomol. 24, 1473–1480 ● Moritz, R.F.A. et al. (2007) The size of wild honeybee populations (Apis mellifera) and its implications for the conservation of honeybees. J. Insect Conserv. 11, 391–397 ● Jaffe´e, R. et al. (2010) Estimating the density of honeybee colonies across their natural range to fill the gap in pollinator decline censuses. Conserv. Biol. 24, 583–593 ● Aizen, M.A. and Harder, L.D. (2009) The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr. Biol. 19, 1–4 ● Rasmont, P. and Mersch, P. (1988) Premie`re estimation de la derive faunique chez les bourdons de la Belgique (Hymenoptera, Apidae). Ann. Soc. R. Zool. Belg 118, 141–147 ● Goulson, D. et al. (2008) Decline and conservation of bumble bees. Annu. Rev. Entomol. 53, 191–208 ● Williams, P.H. and Osborne, J.L. (2009) Bumblebee vulnerability and conservation world-wide. Apidologie 40, 367–387 ● Settele, J. et al. (2008). Climatic risk atlas of European butterflies. BioRisk 1, 1–710, DOI:10.3897/biorisk.1 ● Biesmeijer, J.C. et al. (2006) Parallel declines in pollinators and insectpollinated plants in Britain and the Netherlands. Science 313, 351–354 ● Kremen, C. et al. (2002) Crop pollination from native bees at risk from agricultural intensification. Proc. Natl. Acad. Sci. U. S. A. 99, 16812– 16816 ● Larsen, T.H. et al. (2005) Extinction order and altered community structure rapidly disrupt ecosystem functioning. Ecol. Lett. 8, 538–547 ● Winfree, R. et al. (2009) A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 90, 2068–2076 ● Kleijn, D. and Raemakers, I. (2008) A retrospective analysis of pollen host plant use by stable and declining bumblebee species. Ecology 89, 1811–1823 ● Burd, M. (1994) Bateman principle and reproduction-the role of pollen limitation in fruit and seed set. Bot. Rev. 60, 83–139 ● Fontaine, C. et al. (2006) Functional diversity of plant-pollinator interaction webs enhances the persistence of plant communities. PLoS Biol. 4, e1 DOI:10.1371/journal.pbio.0040001 ● Hegland, S.J. and Totland, Ø. (2008) Is the magnitude of pollen limitation in a plant community affected by pollinator visitation and plant species specialisation levels? Oikos 117, 883–891 ● Bond, W.J. (1994) Do mutualisms matter? Assessing the impact of pollinator and disperser disruption on plant extinction. Proc. R. Soc. Lond. B Biol. Sci. 344, 83–90 ● Bascompte, J. et al. (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312, 431–433 ● Bascompte, J. et al. (2003) The nested assembly of plant animal mutualistic networks. Proc. Natl. Acad. Sci. U. S. A. 100, 9383–9387 ● Memmott, J. et al. (2004) Tolerance of pollination networks to species extinctions. Proc. R. Soc. Lond. B Biol. Sci. 271, 2605–2611 ● Fortuna,M.A. and Bascompte, J. (2006) Habitat loss and the structure of plant–animal mutualistic networks. Ecol. Lett. 9, 278–283 ● Le Conte, Y. and Navajas, M. (2008) Climate change: impact on honey bee populations and diseases. Rev. Sci. Tech. Off. Int. Epizoot. 27, 499– 510 ● Tylianakis, J.M. et al. (2008) Global change and species interactions in terrestrial ecosystems. Ecol. Lett. 11, 1351–1363 ● Aizen, M.A. et al. (2008) Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency. Curr. Biol. 18, 1–4 ● Garibaldi, L.A. et al. (2009) Pollinator shortage and global crop yield - Looking at the whole spectrum of pollinator dependency. Commun. Integr. Biol. 2, 37–39 ● Losey, J.E. and Vaughan, M. (2006) The economic value of ecological services provided by Insects. BioScience 311–323 ● Hoehn, P. et al. (2008) Functional group diversity of bee pollinators increases crop yield. Proc. R. Soc. Lond. B Biol. Sci. 275, 2283–2291 ● Winfree, R. and Kremen, C. (2009) Are ecosystem services stabilized by differences among species? A test using crop pollination. Proc. R. Soc. Lond. B Biol. Sci. 276, 229–237 ● Gallai, N. et al. (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol. Econ. 68, 810–821 ● Didham, R.K. et al. (2007) Interactive effects of habitat modification and species invasion on native species decline. Trends Ecol. Evol. 22, 489–496 ● Oldroyd, B.P. (2007) What’s killing American honey bees? Plos Biol. 5, 1195–1199 ● Schweiger, O. et al. Multiple stressors on biotic interactions: how climate change and alien species interact to affect pollination. Biol. Rev. DOI:10.1111/j.1469-185X.2010.00125.x ● Steffan-Dewenter, I. et al. (2002) Scale-dependent effects of landscape context on three pollinator guilds. Ecology 83, 1421–1432 ● Hendrickx, F. et al. (2007) How landscape structure, land-use intensity and habitat diversity affect components of total arthropod diversity in agricultural landscapes. J. Appl. Ecol. 44, 340–351 ● Kevan, P.G. et al. (1997) Log-normality of biodiversity and abundance in diagnosis and measuring of ecosystemic health: pesticide stress on pollinators on blueberry heaths. J. Appl. Ecol. 34, 1122–1136 ● Rortais, A. et al. (2005) Modes of honeybees exposure to systemic insecticides: estimated amounts of contaminated pollen and nectar consumed by different categories of bees. Apidologie 36, 71–83 ● Thomson, D.M. (2006) Detecting the effects of introduced species: a case study of competition between. Apis and Bombus. Oikos 114, 407– 418 ● Stout, J. and Morales, C.L. (2009) Ecological impacts of invasive alien species on bees. Apidologie 40, 388–409 ● Cox-Foster, D.L. et al. (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318, 283–287 ● Neumann, P. and Carreck, C. (2010) Honey bee colony losses: a global perspective. J. Apic. Res. 49, 1–6 ● Williams, P.H. et al. (2007) Can vulnerability among British bumblebee (Bombus) species be explained by niche position and breadth? Biol. Conserv. 138, 493–505 ● Dormann, C.F. et al. (2008) Prediction uncertainty of environmental change effects on temperate European biodiversity. Ecol. Lett. 11, 235– 244 ● Brown, M.J.F. and Paxton, R.J. (2009) The conservation of bees: a global perspective. Apidologie 40, 410–416 ● Cane, J.H. et al. (2006) Complex responses within a desert bee guild (Hymenoptera: Apiformes) to urban habitat fragmentation. Ecol. Appl. 16, 632–644 ● Carre´, G. et al. (2009) Landscape context and habitat type as drivers of bee diversity in European annual crops. Agric. Ecosyst. Environ. 133, 40–47 ● Winfree, R. et al. (2007) Effect of human disturbance on bee communities in a forested ecosystem. Conserv. Biol. 21, 213–223 ● Winfree, R. et al. (2008) Wild bee pollinators provide the majority of crop visitation across land-use gradients in New Jersey and Pennsylvania, USA. J. Appl. Ecol. 45, 793–802 ● Steffan-Dewenter, I. et al. (2006) Bee diversity and plant-pollinator interactions in fragmented landscapes. In Specialization and Generalization in Plant-Pollinator Interactions (Waser, N.M. and Ollerton, J., eds), pp. 387–410, University of Chicago Press ● Brosi, B.J. et al. (2008) The effects of forest fragmentation on bee communities in tropical countryside. J. Appl. Ecol. 45, 773–783 ● Donaldson, J. et al. (2002) Effects of habitat fragmentation on pollinator diversity and plant reproductive success in renosterveld shrublands of South Africa. Conserv. Biol. 16, 1267–1276 ● Tscharntke, T. et al. (2002) Contribution of small habitat fragments to conservation of insect communities of grassland-cropland landscapes. Ecol. Appl. 12, 354–363 ● Westrich, P. (1996)Habitat requirements of central European bees and the problems of partial habitats. In The Conservation of Bees (Matheson, A., et al. eds), pp 1–16, Academic Press ● Pauw, A. (2007) Collapse of a pollination web in small conservation areas. Ecology 88, 1759–1769 ● Kremen, C. et al. (2007) Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land use change. Ecol. Lett. 10, 219–314 ● Alston, D.G. et al. (2007) Effects of the insecticide Phosmet on solitary bee foraging and nesting in orchards of Capitol Reef National Park, Utah. Environ. Entomol. 36, 811–816 ● Brittain, C.A. et al. (2010) Impacts of a pesticide on pollinator species richness at different spatial scales. Basic Appl. Ecol. 11, 106–115 ● Gabriel, D. and Tscharntke, T. (2007) Insect pollinated plants benefit from organic farming. Agric. Ecosyst. Environ. 118, 43–48 ● Holzschuh, A. et al. (2008) Agricultural landscapes with organic crops support higher pollinator diversity. Oikos 117, 354–361 ● Thompson, H.M. and Hunt, L.V. (1999) Extrapolating from honeybees to bumblebees in pesticide risk assessment. Ecotoxicology 8, 147– 166 ● Morandin, L.A. et al. (2005) Lethal and sub-lethal effects of spinosad on bumble bees (Bombus impatiens Cresson). Pest Manag. Sci. 61, 619– 626 ● Lavergne, S. et al. (2006) Fingerprints of environmental change on the rare Mediterranean flora: a 115-year study. Glob. Change Biol. 12, 1466–1478 ● Carvell, C. et al. (2006) Declines in forage availability for bumblebees at a national scale. Biol. Conserv. 132, 481–489 ● Westphal, C. et al. (2003) Mass flowering crops enhance pollinator densities at a landscape scale. Ecol. Lett. 6, 961–965 ● Lambdon, P.W. et al. (2008) Alien flora of Europe: species diversity, temporal trends, geographical patterns and research needs. Preslia 80, 101–149 ● Traveset, A. and Richardson, D.M. (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol. Evol. 21, 208–216 Review Trends in Ecology and Evolution Vol.25 No.6 352 ● Matsumura, C. et al. (2004) Invasion status and potential ecological impacts of an invasive alien bumblebee, Bombus terrestris L. (Hymenoptera: Apidae) naturalized in Southern Hokkaido, Japan. Glob. Environ. Res. 8, 51–66 ● Steffan-Dewenter, I. and Tscharntke, T. (2000) Resource overlap and possible competition between honey bees and wild bees in central Europe. Oecologia 122, 288–296 ● Roubik, D.W. and Wolda, H. (2001) Do competing honey bees matter? Dynamics and abundance of native bees before and after honey bee invasion. Popul. Ecol. 43, 53–62 ● Goulson, D. and Sparrow, K. (2009) Evidence for competition between honeybees and bumblebees; effects on bumblebee worker size. J. Insect Conserv. 13, 177–181 ● Franck, P. et al. (1998) The origin of west European subspecies of honeybees (Apis mellifera): new insights from microsatellite and mitochondrial data. Evolution 52, 1119–1134 ● Anderson, D. and East, I.J. (2008) The latest buzz about Colony Collapse Disorder. Science 319, 724–725 ● Watanabe, M.E. (2008) Colony collapse disorder: many suspects, no smoking gun. Bioscience 58, 384–388 ● Woolhouse, M.E.J. et al. (2005) Emerging pathogens: the epidemiology and evolution of species jumps. Trends Ecol. Evol. 20, 238–244 ● Ribie`re, M. et al. (2008) Natural history and geographical distribution of honey bee viruses. In Virology and the Honey Bee (Aubert, M.F.A. et al., eds), pp. 15–84, European Commission ● Ongus, J.R. et al. (2004) Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor. J. Gen. Virol. 85, 3747–3755 ● Eyer, M. et al. (2009) Small hive beetle, Aethina tumida, as a potential biological vector of honeybee viruses. Apidologie 40, 419–428 ● Genersch, E. et al. (2006) Detection of deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities. J. Invertebr. Pathol. 91, 61–63 ● Goulson, D. (2003) Effects of introduced bees on native ecosystems. Annu. Rev. Ecol. Syst. 34, 1–26 ● Neumann, P. and Elzen, P.J. (2004) The biology of the small hive beetle (Aethina tumida, Coleoptera: Nitidulidae): gaps in our knowledge of an invasive species. Apidologie 35, 229–247 ● Spiewok, S. and Neumann, P. (2006) Infestation of commercial bumblebee (Bombus impatiens) field colonies by small hive beetles (Aethina tumida). Ecol. Entomol. 31, 623–628 ● Hickling, R. et al. (2006) The distributions of a wide range of taxonomic groups are expanding polewards. Glob. Change Biol. 12, 450–455 ● Stone, G.N. and Willmer, P.G. (1989) Warm-up rates and body temperatures in bees - the importance of body size, thermal regime and phylogeny. J. Exp. Biol. 147, 303–328 ● Hegland, S.J. et al. (2009) How does climate warming affect plant– pollinator interactions? Ecol. Lett. 12, 184–195 ● Parmesan, C. et al. (1999) Poleward shifts in geographical ranges of butterfly species associated with regionalwarming. Nature 399, 579–583 ● Thomas, C.D. et al. (2001) Ecological and evolutionary processes at expanding range margins. Nature 411, 577–581 ● Memmott, J. et al. (2007) Global warming and the disruption of plant– pollinator interactions. Ecol. Lett. 10, 710–717 ● Schweiger, O. et al. (2008) Climate change can cause spatial mismatch of trophic interacting species. Ecology 89, 3472–3479 ● Ellis, J.D. and Munn, P.A. (2005) The worldwide health status of honey bees. Bee World 86, 88–101 ● Pilling, E.D. and Jepson, P.C. (1993) Synergism between EBI fungicides and a pyrethroid insecticide in the honeybee (Apis mellifera). Pestic. Sci. 39, 293–297 ● Chen, Y.P. and Siede, R. (2007) Honeybee viruses. Adv. Virus Res. 70, 33–80 Review Trends in Ecology and Evolution Vol.25 No.6 353